1 Selective brain cooling in Arabian oryx (Oryx leucoryx)

25 Pages·2012·0.19 MB·English

3917
The Journal of Experimental Biology 215, 3917-3924
© 2012. Published by The Company of Biologists Ltd
doi:10.1242/jeb.074666
RESEARCH ARTICLE
Selective brain cooling in Arabian oryx (Oryx leucoryx): a physiological mechanism
for coping with aridity?
Robyn S. Hetem1,*, W. Maartin Strauss1–3, Linda G. Fick1, Shane K. Maloney1,4, Leith C. R. Meyer1,
Andrea Fuller1, Mohammed Shobrak2,5and Duncan Mitchell1
1Brain Function Research Group, School of Physiology, University of the Witwatersrand, 7 York Road, Parktown 2193, South Africa,
2National Wildlife Research Center, Saudi Wildlife Commission, PO Box 1086, Taif, Saudi Arabia, 3Department of Environmental
Sciences, Unisa, Private Bag X6, Florida, 1709, South Africa, 4School of Anatomy, Physiology and Human Biology, University of
Western Australia, Stirling Highway, Crawley 6009, Western Australia and 5Biology Department, Science College, Taif University,
PO Box 888, Taif, Saudi Arabia
*Author for correspondence ([email protected])
SUMMARY
Selective brain cooling is a thermoregulatory effector proposed to conserve body water and, as such, may help artiodactyls cope
with aridity. We measured brain and carotid blood temperature, using implanted data loggers, in five Arabian oryx (Oryx leucoryx)
in the desert of Saudi Arabia. On average, brain temperature was 0.24±0.05°C lower than carotid blood temperature for four oryx
in April. Selective brain cooling was enhanced in our Arabian oryx compared with another species from the same genus (gemsbok
Oryx gazella gazella) exposed to similar ambient temperatures but less aridity. Arabian oryx displayed a lower threshold
(37.8±0.1°C vs 39.8±0.4°C), a higher frequency (87±6% vs15±15%) and a higher maximum magnitude (1.2±0.2°C vs0.5±0.3°C) of
selective brain cooling than did gemsbok. The dominant male oryx displayed less selective brain cooling than did any of the other
oryx, but selective brain cooling was enhanced in this oryx as conditions became hotter and drier. Enhanced selective brain
cooling in Arabian oryx supports the hypothesis that selective brain cooling would bestow survival advantages for artiodactyl
species inhabiting hot hyper-arid environments.
Key words: brain temperature, artiodactyl, biologging, desert.
Received 4 May 2012; Accepted 7 August 2012
INTRODUCTION places the Ruminantiamorpha/Suinamorpha/Camelidamorpha
Artiodactyla, an evolutionarily successful and hugely speciose order divergence before the appearance of the Tragulidae within the
of large ungulates, with 90 extant genera, evolved during the Eocene Ruminantiamorpha (Spaulding et al., 2009), making it likely that the
and speciated during a warming period in the Mid-Miocene Climatic absence of the rete in Tragulidae has been a secondary loss. Thus,
Optimum (Barnosky et al., 2003). Since they evolved in conditions the carotid rete in the Artiodactyla lineage probably evolved at about
that were hotter and drier than present, artiodactyls may be pre- the same time as the rumen, during the mid-Miocene, about 20Mya.
adapted to cope with warmer and drier environments than those Selective brain cooling was originally hypothesized to primarily
currently experienced (Barnosky et al., 2003; Mitchell and Lust, protect the brain during rises in body temperature (Baker, 1979;
2008). Traditionally, the success of artiodactyls has been attributed Mitchell et al., 1987). However, recent studies support an alternative
to the evolution of improved locomotion and the ruminant digestive concept, namely that mammals possessing a carotid rete may employ
tract, adaptations which allowed these ungulates to use widely selective brain cooling to attenuate the drive for evaporative cooling
dispersed forage with a high fibre content (Janis, 1989; Codron et in arid conditions. Selective brain cooling reduces the drive from
al., 2008). Recently, however, another potential contributor to their temperature-sensitive neurones in the hypothalamus on evaporative
success has been proposed: the evolution of the carotid rete and the heat dissipation and conserves body water by switching body heat
use of selective brain cooling (Fuller et al., 2008; Mitchell and Lust, loss to non-evaporative avenues (Jessen et al., 1994; Mitchell et al.,
2008). The carotid rete consists of an intertwining network of 1997; Fuller et al., 1999; Maloney et al., 2002; Mitchell et al., 2002).
arterioles that lies within a venous sinus at the base of the brain. Abolition of selective brain cooling, which can occur rapidly, allows
Venous blood cooled by evaporation from the nasal mucosa drains evaporative heat loss to be restored in thermal emergencies, such
into the sinus and so cools the arterial blood destined for the brain, as flight from a predator (Jessen, 1998; Mitchell et al., 2002). So,
generating selective brain cooling (Baker, 1982; Mitchell et al., 1987) selective brain cooling would have survival advantages for
– the reduction of brain temperature below arterial blood temperature artiodactyls, not available to perissodactyls, in environments in
(IUPS Thermal Commission, 2003). The rete is absent in the closest which water resources are limited and unpredictable (Mitchell et
relatives to the artiodactyls, the perissodactyls, absent in the oldest al., 2002).
ruminant group, the Tragulidae (Fukuta et al., 2007), but is present If the evolution of the carotid rete indeed promoted
in each of the artiodactyl clades: Ruminantiamorpha, Suinamorpha thermoregulatory flexibility and thus facilitated artiodactyl invasion
and Camelidamorpha. Recent systematic analysis of the Artiodactyla of arid zones during the highly seasonal post-Eocene world (Mitchell
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3918 The Journal of Experimental Biology 215 (22)
and Lust, 2008), selective brain cooling may be a key adaptation iodine antiseptic (Vetedine; Vetoquinol Veterinary Pharmaceuticals,
allowing artiodactyls to cope with the increasing aridity and heat Lure, France). For the measurement of carotid arterial blood
stress that is occurring with climate change (Fuller et al., 2008). temperature, a thermistor inserted in a blind-ended and thin-walled
However, not all artiodactyl species exhibit the same capacity for polytetrafluoroethylene (PTFE) catheter (o.d. 1.35mm, i.d. 0.97mm;
selective brain cooling. The absence of the rete in primitive Straight Aortic Flush 4F Catheter; Cordis, the Netherlands) was
artiodactyls, such as the mouse deer [Tragulus javanicus, Tragulus advanced 60mm into the left common carotid artery towards the
napu(Fukuta et al., 2007)], might be expected to decrease the water heart, at a position midway along the length of the neck, and secured
economy of these species and restrict them to habitats where water with a purse-string suture in the arterial wall. Outside the artery,
scarcity is not an issue. Indeed, the mouse deer is restricted to the PTFE tube was sealed on a Teflon®-coated co-axial cable
climatically stable forest environments (Whittow et al., 1977). By (150mm long, o.d. 3mm; Belden, Richmond, IN, USA) connecting
contrast, enhanced selective brain cooling may be expected in the thermistor to the temperature-sensitive data logger (see
artiodactyl species inhabiting hot hyper-arid environments. Arabian temperature measurements). The data logger was positioned
oryx (Oryx leucoryx) inhabit one of the hottest deserts in the world, subcutaneously, dorsal to the artery. For measurement of brain
in Saudi Arabia, and survive most of the year, including the hottest temperature, a second data logger was positioned subcutaneously,
summer months, without access to drinking water. To investigate caudal to the base of the left ear. Its Teflon®-coated cable was
the status of their selective brain cooling, we employed implanted advanced subcutaneously over the skull, where it was connected to
data loggers to measure brain and carotid arterial blood temperatures a thermistor housed in a head plate and guide tube. The guide tube,
of five free-living Arabian oryx in their natural habitat. Brain and constructed from cellulose acetate butyrate tubing (40mm long, o.d.
carotid blood temperature have not been measured in Arabian oryx 1.95mm, i.d. 1mm; World Precision Instruments, Sarasota, FL,
previously but have been measured in another member of the same USA) sealed at the tip by a steel cap, was inserted through a 2mm-
genus, the gemsbok [Oryx gazella gazella(Maloney et al., 2002)]. diameter burr hole, which was drilled through the cranium, at co-
Gemsbok inhabit hot dry environments in southern Africa, and ordinates pre-determined from head sections of dead oryx of similar
indeed were studied at ambient temperatures similar to those size, so that the probe tip would be positioned near the hypothalamus.
experienced by our Arabian oryx, but the rainfall experienced by The polyvinyl chloride head plate (20(cid:3)10(cid:3)5mm) was secured to
our Arabian oryx was one-third of that experienced by the gemsbok. the skull by two bone screws and covered by skin.
The wounds were treated with a topical antiseptic spray
MATERIALS AND METHODS (Necrospray; Centaur Labs, Johannesburg, South Africa). Each oryx
Animals and habitat received a long-acting antibiotic (450mg i.m. penicillin, Norocillin
The study took place between March and July 2006 within the La; Norbrook Laboratories Ltd, Newry, Northern Ireland), a non-
2200km2Mahazat as-Sayd Protected Area (22°25(cid:2)N, 41°48(cid:2)E) in steroidal anti-inflammatory analgesic (100mg i.m. phenylbutazone,
the open steppe desert in Saudi Arabia, which is both the historical dexaphenylarthrite injectable solution; Vetoquinol Veterinary
and the current habitat for Arabian oryx (Oryx leucoryxPallas 1777). Pharmaceuticals), a long-acting parasiticide (2ml s.c. Ivermectin,
Adult, wild-born oryx (two male and two female) were captured in Noromectin; Norbrook Laboratories Ltd) and a multivitamin
the Protected Area in mid-March 2006. The oryx were habituated injection (9ml i.m.Multivit injectable solution; Univet Ltd, County
in outdoor pens for two weeks to reduce potential peri-operative Cavan, Ireland). Before anaesthesia was terminated, we fitted a neck
stress. An additional male oryx was obtained from the breeding herd collar containing a tracking radio transmitter (MOD-500; Telonics,
at the National Wildlife Research Center in Taif (21°15(cid:2)N, 40°42(cid:2)E). Inc., Mesa, AZ, USA).
This male oryx remained in Taif in a partially shaded pen throughout Following surgery, the oryx were transported back to their pens,
the study period and had lucerne and water available ad libitum. where they became ambulatory within ~10min after the effects of
All experimental procedures were approved by the Animal Ethics etorphine were reversed with diprenorphine hydrochloride [7.5mg
Screening Committee of the University of the Witwatersrand intravenously (i.v.) M5050; C-Vet]. The oryx at Taif remained in
(protocol no. 2005/87/5). its pen for the duration of the study. Two weeks after surgery, the
four oryx in the Mahazat as-Sayd Protected Area were released into
Surgery a 2km2 fenced enclosure with natural forage and water available
The oryx, at both locations, were darted and anaesthetized in their ad libitum. Ten days later, they were allowed to enter and range
holding pens with etorphine hydrochloride [2.5mg intramuscularly freely within the Mahazat as-Sayd Protected Area, where they were
(i.m.), M99; C-Vet, Leyland, UK] and, once recumbent, were left undisturbed, apart from the occasional serendipitous visual
transported to a temporary operating theatre within 200m of the contact by rangers. The four oryx separated from each other shortly
pens. At this theatre, the animals were placed in sternal recumbency, after their release, with some joining other oryx in the reserve.
with their heads elevated. The animals were intubated, and A year after surgery, the four oryx were radio tracked, captured
anaesthesia was maintained with 2–6% isoflurane (Aerrane; Astra and transported back to the holding pens. Those oryx, and the one at
Zeneca, Johannesburg, South Africa) administered in 100% oxygen. Taif, were anaesthetized again and the data loggers were removed
Respiratory rate, heart rate, arterial oxygen saturation and rectal under a surgical procedure similar to that used for the original
temperature were monitored throughout the surgery, which lasted implantation. The surgical wounds had healed and there were no signs
about two hours. of infection. After two weeks of recovery in pens, the four free-living
Under sterile surgical conditions, we implanted temperature- oryx were re-released into the Mahazat as-Sayd Protected Area.
sensitive data loggers (see below) with sensors in the brain and
carotid artery. The loggers were dry sterilized in formaldehyde Temperature measurements
vapour before implantation. After we had administered a local The miniature thermometric data loggers (StowAway XTI; Onset
anaesthetic [3ml 2% lignocaine hydrochloride; Bayer Animal Computer, Pocasset, MA, USA) had outside dimensions of
Health (Pty) Ltd, Isando, South Africa] subcutaneously (s.c.) at the ~50(cid:3)45(cid:3)20mm and a mass of ~40g when covered in inert wax
incision sites, the sites were shaved and sterilized with povidone (Sasol, Johannesburg, South Africa). Temperature sensors used to
THE JOURNAL OF EXPERIMENTAL BIOLOGY
Selective brain cooling in Arabian oryx 3919
measure brain and carotid blood temperatures were constructed from availability and carotid blood temperature on the average 24-h
ruggedized glass-coated bead thermistors with insulated extension selective brain cooling (difference between carotid blood and brain
leads (bead diameter 0.3mm; AB0E3-BR11KA103N; temperatures). Water availability was a categorical predictor and
Thermometrics, Edison, NJ, USA). The loggers had a resolution of divided our data into four periods: (1) water was freely available
0.04°C and a measurement range from +34°C to +46°C. The scan and the oryx drank daily, (2) water was freely available and the
interval of the loggers was set at 5min. Each sensor assembly was oryx drank weekly, (3) limited free-standing water (7mm rain in
calibrated against a high-accuracy thermometer (Quat 100; Heraeus, May) and (4) no free-standing water (0mm rain in June). We
Hanau, Germany) in an insulated water bath. After calibration, the controlled for repeated measurements by including ‘individual’ and
loggers and their sensors measured blood and brain temperatures ‘day of the year’ as random factors. To account for potential
to an accuracy better than 0.05°C. autocorrelation between our variables, we included a first-order
autoregressive process (AR1) in our model structure. We generated
Climatic data measurements 16 models (1 full model, 1 null model and 14 reduced models) based
We collected climatic data from a portable weather station erected on all additive term combinations and determined the best-fit model
near the Mahazat as-Sayd Protected Area, at the Saja/Umm ar-Rimth based on the Akaike’s Information Criterion (AIC). Models
Protected Area (23°22(cid:2)N, 42°45(cid:2)E), and also at the National presenting with AICgreater than two were not considered plausible
Wildlife Research Center in Taif. We recorded wind speed (ms–1), models (Burnham and Anderson, 2002).
solar radiation (Wm–2), dry-bulb temperature (°C) and relative Values are expressed as means ± s.d., and P<0.05 was considered
humidity (%). We also recorded black globe temperature (°C) and significant.
rainfall on site at the Mahazat as-Sayd Protected Area for the
duration of the study period. Black globe temperature provides an RESULTS
index of the thermal load on an animal as it integrates the effects Climate
of radiant and convective heat exchange. Air and black globe temperatures varied as a function of the time
of day, peaking just after solar noon (12:00) and reaching a
Data analysis minimum just before sunrise (Fig.1). Air and black globe
Although we recovered the data a year after surgery, we analysed temperatures increased progressively from April (when all rain fell)
responses for a period when we had the most complete data set. to June (when no rain fell) (Table1). Despite a difference in the
The data loggers that measured carotid blood temperature in three number of days over which selective brain cooling was recorded
of the oryx (identified as Oryx 1, Oryx 2 and Oryx 3) malfunctioned for each oryx in April, there was no difference in the 24-h air
within a month after surgery (after a minimum of 4400 simultaneous temperatures experienced by the four oryx (F3.842.0, P0.12). Solar
measurements of brain and carotid blood temperature). The data radiation showed the expected bell-shaped distribution and peaked
logger that measured brain temperature in the captive male oryx in at 1034±64Wm–2around solar noon in the month in which we had
Taif (identified as Taif oryx) malfunctioned within a month after the most complete selective brain cooling data set (April). Wind
surgery (after ~7900 simultaneous measurements of brain and speed increased to a maximum of 9.4±2.1ms–1in the late afternoon
carotid blood temperatures). We obtained brain temperature and and averaged 4.6±1.5ms–1over the 24-h periods during April. Mean
carotid blood temperature data from the other free-living male oryx 24-h vapour pressure and relative humidity decreased progressively
(identified as Oryx 4) for four months after surgery (~16,500 from April to June (Table1). Rainfall totalled 31mm during 2006,
simultaneous measurements of brain and carotid blood substantially lower than the 10-year average of 100±60mm. April
temperatures), but his brain temperature probe exhibited an was the wettest month (17mm) but some rain fell during March
intermittent fault that restricted data analysis to two months. Despite (7mm) and May (7mm). Because surgery was completed in late
the fault, the data from this animal allowed us to compare selective March, we have excluded data for March from our analysis to
brain cooling over two seasonal periods. Furthermore, the eliminate any possible post-surgical abnormalities in responses.
opportunity presented itself to compare a dominant male with a
subordinate male exposed to similar environmental conditions. Selective brain cooling
We compared variables of the nycthemeral rhythm of brain and Brain and carotid blood temperatures exhibited a nycthemeral
carotid blood temperatures with paired t-tests. We analyzed the rhythm with a trough between 06:00 and 07:00 (following sunrise)
relationship between brain temperature and carotid blood
temperature by sorting all five-minute measurements of carotid
blood temperature into 0.1°C classes and determining the mean, 45
standard deviation, maximum and minimum brain temperature at C)
each class of carotid blood temperature. We determined the threshold e (° 35
for selective brain cooling as the point at which the regression line ur
of brain temperature against carotid blood temperature intercepted erat 25
the line of identity (yx). Selective brain cooling was calculated as mp
the difference between carotid blood and brain temperature, with e
positive values indicating selective brain cooling. The maximum Air t 15
positive difference was defined as maximum selective brain cooling
capacity. Mean selective brain cooling was calculated as the average 00:00 06:00 12:00 18:00
positive difference, and the frequency of selective brain cooling was Time of day
calculated as the proportion of positive values.
Fig.1. Average 24 h pattern of air temperature (mean ± s.d.) during May
We used mixed effects linear models (function ‘lme’ using the
(light grey line) and June (black line). The shaded grey area represents the
statistical package ‘R’) (R Development Core Team, 2008) to
range of air temperature to which each of the four oryx were exposed for
investigate the effect of air temperature, water vapour pressure, water the period during which we collected selective brain cooling data in April.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3920 The Journal of Experimental Biology 215 (22)
Table 1. Environmental conditions (mean ± s.d.) during the three months in which the oryx were living free in the Mahazat as-Sayd
Protected Area
April May June
Air temperature (°C)
24 h mean 25.0±3.6 30.5±1.7 33.7±0.9
24 h minimum 17.2±4.1 22.7±1.9 25.3±1.7
24 h maximum 31.4±3.5 36.9±1.9 40.2±1.0
Black globe temperature (°C)
24 h mean 31.7±3.0 35.4±2.9 38.1±1.4
24 h minimum 16.4±3.2 20.0±2.3 21.5±2.8
24 h maximum 51.0±5.6 55.0±4.3 57.9±3.3
Mean 24 h vapour pressure (kPa) 0.81±0.26 0.79±0.28 0.44±0.05
Relative humidity (%) 25±10 20±9 9±1
Mean 24 h wind speed (ms–1) 4.6±1.5 4.2±1.3 4.1±1.0
Mean 24 h radiation (Wm–2) 286±50 289±46 312±12
Total rainfall (mm) 17 7 0
and a peak between 17:00 and 18:00 (shortly before sunset) (Fig.2). Fig.3 shows brain temperature as a function of carotid blood
During April, in four animals (i.e. excluding Oryx 4), the mean 24- temperature (upper panels in A–D) and the frequency distribution
h brain temperature was lower than carotid blood temperature of carotid blood temperature (lower panels in A–D) in two male
(38.45±0.06°C vs38.70±0.10°C; t311.5, P0.0014). Minimum 24- oryx while both had access to food and water; the male in Taif drank
h brain and carotid blood temperatures were similar (37.36±0.28°C water daily (Fig.3B) whereas the male (Oryx 3) in the Mahazat as-
vs37.53±0.34°C; t30.99, P0.39), while the maximum 24-h brain Sayd Protected Area drank less frequently (Fig.3A). The captive
temperature was significantly lower than carotid blood temperature male oryx (Taif oryx) employed selective brain cooling less
(39.34±0.28°C vs39.61±0.20°C; t34.2, P0.024). On average, the frequently (81% vs94%) than did the free-living male oryx (Oryx
oryx implemented selective brain cooling throughout the day, 3), despite the two oryx having the same carotid blood temperature
except for the period after sunrise (Fig.2). For the four oryx, brain and threshold of selective brain cooling (Table2).
temperature was lower than carotid blood temperature, measured Oryx 4, a male that was frequently observed pacing the fence
simultaneously, 87±6% of the time. On average, brain temperature while in captivity, initiating fights with other males and squat-
was 0.24±0.05°C lower than carotid blood temperature for these defecating, behaviours typical of a dominant male (Stanley Price,
four oryx in April. Mean selective brain cooling, the average 1989), displayed less selective brain cooling than did any of the
difference between carotid blood and brain temperature when the other oryx (Table2). Compared with Oryx 3, a male that appeared
oryx were implementing selective brain cooling, was 0.32±0.03°C, to us to be a subordinate, the dominant male (Oryx 4) showed a
and the maximum magnitude of selective brain cooling was higher threshold of selective brain cooling (39.6°C vs37.8°C), a
1.15±0.17°C. The threshold for selective brain cooling, defined as lower maximum magnitude of selective brain cooling (0.93°C vs
the point at which carotid blood and mean brain temperatures were 1.35°C) and implemented selective brain cooling less frequently
equal, was 37.8±0.1°C (mean ± s.d., N4, Table2). (11% vs 94%) (Table2). Unlike that of the other oryx (Fig.2),
A B Fig.2. Average 24 h rhythm of brain (grey line) and
40 40 carotid blood (black line) temperatures for two
Oryx 1 Oryx 2 female (A,B) and two male (C,D) oryx in April. All
Carotid oryx had access to food and water ad libitum. Black
39 39 horizontal bars indicate night-time.
Carotid
Brain
38 Brain 38
C) 37 37
°
e (
ur 00:00 06:00 12:00 18:00 00:00 06:00 12:00 18:00
at
er C D
mp 40 40
Te Oryx 3 Taif oryx
Carotid
39 39
Carotid
Brain
38 38 Brain
37 37
00:00 06:00 12:00 18:00 00:00 06:00 12:00 18:00
Time of day
THE JOURNAL OF EXPERIMENTAL BIOLOGY
Selective brain cooling in Arabian oryx 3921
Table 2. Mean brain and carotid blood temperatures recorded every 5 min and the mean difference between carotid blood (T )
carotid
and brain (T ) temperatures, as well as the mean, maximum, frequency and threshold for selective brain cooling in three male and two
brain
female oryx
Selective brain cooling
Mean brain Mean carotid Mean Tcarotid–
Oryx Month temperature (°C) temperature (°C) Tbrain(°C) Mean (°C) Max (°C) Frequency (%) Threshold (°C) N (days)
Oryx 1 (cid:2) April 38.42±0.31 38.63±0.39 +0.21±0.19 0.29±0.16 0.95 90 37.9 15
Oryx 2 (cid:2) April 38.44±0.62 38.64±0.74 +0.20±0.26 0.30±0.19 1.10 82 37.6 24
Oryx 3 (cid:3) April 38.53±0.38 38.83±0.50 +0.30±0.20 0.34±0.17 1.35 94 37.8 22
Oryx 4 (cid:3) May 38.99±0.45 38.71±0.60 –0.28±0.25 0.18±0.14 0.93 11 39.6 28
June 38.87±0.88 38.86±1.11 –0.03±0.32 0.32±0.19 1.03 38 39.0 29
Taif oryx (cid:3) April 38.41±0.45 38.66±0.60 +0.24±0.26 0.35±0.20 1.19 81 37.9 27
Data are means ± s.d. and encompass at least 4400 simultaneous measurements of brain and carotid blood temperature in each animal. N number of days
of data.
the brain temperature of the dominant male oryx (Oryx 4) was (Fig.3D). His brain temperature was an average of 0.28±0.25°C
generally above that of his carotid blood temperature, particularly higher than his carotid blood temperature during May, and only
at low body temperatures in May (Fig.4A), when climatic 0.03±0.32°C higher during June.
conditions were relatively mild and drinking water was available These differences in selective brain cooling between May and
through ephemeral pools of rainwater. But selective brain cooling June were not simply the result of a higher carotid blood temperature
was enhanced in Oryx 4 when conditions were hotter and drier during June. When analysed over the same carotid blood temperature
in June (Fig.4B). Although Oryx 4 spent only 11% of the time range (37–40°C), both the frequency of selective brain cooling (30%)
with his hypothalamus cooler than his carotid blood during May and the average difference between carotid blood and brain
(Fig.3C), this frequency increased to 38% of the time in June temperatures (0.06±0.30°C) indicated enhanced selective brain
A B Fig.3. Brain temperature as a function of carotid
blood temperature (top panels in A–D) and the
41 Oryx 3 ♂ 41 Taif oryx ♂ frequency distribution of carotid blood
amice (°C) 39 39 toaernmyimxp a(eOlrsar ythuxar ed3 (aabcnocdtet otshmse t poTa afnoifeo oldsr yainxn) d,A w–wDhae)t eninr b atowdtho male
Hypothalmperatur 37 37 lwJibuhintiuleem. fEr, eaaecn hdra 5an- gmfirneinge -rilneiv citnohgred midnegas leoe fro tc riaynxr oM (tOiadyr yb axlon 4od)d ,in
e temperature was sorted into 0.1°C classes, and
t
the mean (solid black line), minimum (lower
35 35
grey line) and maximum (upper grey line) brain
37 39 41 37 39 41
temperatures were calculated for each 0.1°C
y 600 600 class of carotid blood temperature. The broken
c line represents the line of identity; points below
uen 400 400 this line reflect selective brain cooling. Lower
eq 200 200 panels in A–D show the absolute frequencies
Fr 0 0 with which each 0.1°C class of blood
37 39 41 37 39 41 temperature occurred; 6491 data points were
obtained for the free-living male oryx (Oryx 3),
C D 7968 data points for the captive male oryx in
Taif (Taif oryx), 8067 data points for the free-
41 Oryx 4 ♂ (M ay) 41 Oryx 4 ♂ ( June) living male oryx (Oryx 4) in May and 8355 data
alamicure (°C) 39 39 pseolienctsti vine Jburanien. cAororoliwngs. indicate the threshold of
Hypothmperat 37 37
e
t
35 35
37 39 41 37 39 41
y 600 600
c
en 400 400
u
eq 200 200
Fr 0 0
37 39 41 37 39 41
Carotid temperature (°C)
THE JOURNAL OF EXPERIMENTAL BIOLOGY
3922 The Journal of Experimental Biology 215 (22)
A DISCUSSION
42 Our study provides the first remote and continuous measurement
Oryx 4 ♂ (M ay)
of brain and carotid blood temperatures of Arabian oryx (Oryx
Brain
leucoryx) in their natural habitat, the deserts of Saudi Arabia. Brain
40
temperature was generally below carotid blood temperature near
the peak of the endogenous nycthemeral rhythm of body
38 temperature. However, selective brain cooling was not obligatory
Carotid at high body temperatures; on occasion, brain temperature reached
C) 36 4411..22°°CC .w Dheesnp itthee tchoer raemsppolintuddineg o cfa trhoeti dn ybcltohoedm teermalp erhrayttuhrme wofa sb aralsion
°
e ( 1 2 3 4 and carotid blood temperature of our oryx being similar to that
ur
at B measured in other species (~2°C), selective brain cooling appeared
er to be enhanced in our Arabian oryx. The degree of selective brain
p 42
em Oryx 4 ♂ (J une) Carotid cooling can be measured in three ways, namely the magnitude of
T
the difference between carotid blood and brain temperature, the
40 threshold at which selective brain cooling is implemented, and the
proportion of time spent using selective brain cooling. Our Arabian
oryx, which were exposed to drier natural conditions than any
38
previous animals in which selective brain cooling has been
Brain
measured, displayed a high maximum magnitude of selective brain
36 cooling (1.15°C), a low threshold for selective brain cooling
(37.8°C) and a high frequency of selective brain cooling (87%).
1 2 3 4
The view that selective brain cooling would be enhanced under
Time (days)
dry conditions is supported by our finding that selective brain cooling
was observed more frequently in the free-living male oryx (Oryx
Fig.4. Brain (grey line) and carotid blood (black line) temperatures of the
3), which drank infrequently, than in the captive male oryx (Taif
dominant free-living male oryx (Oryx 4) over a four-day period in May when
oryx), which drank daily, despite the two oryx being exposed to
mean ambient temperature was 27.9±2.0°C (A) and a four-day period in
June when mean ambient temperature was 34.7±0.5°C (B). No rain fell in similar ambient temperatures and having the same carotid blood
June. temperature. Furthermore, under hot and dry conditions (in June),
male Oryx 4 decreased the threshold at which selective brain cooling
was implemented compared with that in May, thereby increasing
cooling during the dry June period compared with May. The the range of body temperatures over which selective brain cooling
threshold for selective brain cooling in Oryx 4 decreased with was implemented and thus increasing the frequency of selective brain
increasing ambient temperature and aridity, from 39.6°C in May to cooling (Fig.3D). The enhanced selective brain cooling was driven
39.0°C in June. Above the threshold, the difference between carotid primarily by water availability (drinking frequency), but carotid
blood and brain temperatures was higher in June (0.28±0.24°C) than blood temperature and water vapour pressure also influenced 24-h
during May (0.16±0.20°C). Nevertheless, the maximum magnitude selective brain cooling (Table3).
of selective brain cooling was similar in May (0.93°C) and June Our conclusions about the enhancement of selective brain cooling
(1.03°C), and selective brain cooling seldom exceeded 1°C at any by aridity seem robust, but our conclusions about seasonal
time. differences in selective brain cooling in the arid-adapted oryx are
The mixed effects linear models allowed us to differentiate the tentative, because we obtained data from only a single male oryx
effects of air temperature and aridity and confirmed that water (Oryx 4) under hot and dry conditions (June). Since non-thermal
availability (drinking frequency) was the best predictor for mean factors affecting sympathetic tone may override the thermal
24-h selective brain cooling, with the top five models all regulation of brain temperature (Kuhnen and Jessen, 1994; Maloney
incorporating water availability (Table3). The best model et al., 2001), particularly in free-living animals (Jessen et al., 1994;
incorporated the effects of water availability, carotid temperature Maloney et al., 2002; Caputa, 2004), high vigilance, and consequent
and water vapour pressure. Among tested explanatory variables, air high sympathetic tone, may have acted to decrease the degree of
temperature had no measurable effect on mean 24-h selective brain selective brain cooling in the dominant male oryx. His frequency
cooling; the addition of air temperature to the model changed the of selective brain cooling was lower, and his threshold of selective
AIC value by more than two (Burnham and Anderson, 2002). brain cooling was higher, than that of all the other oryx measured
Table 3. Akaikeʼs Information Criterion (AIC) for the five best-fit mixed effects linear models incorporating the main factors that accounted for
the variability in average 24-h selective brain cooling
Formula (fixed effects) d AIC AIC
Water availability + water vapour pressure + carotid blood temperature 5 –364.00 0.00
Water availability + water vapour pressure + carotid blood temperature + air temperature 6 –356.66 7.62
Water availability + carotid blood temperature 4 –351.34 12.95
Water availability + carotid blood temperature + air temperature 5 –349.22 15.07
Water availability + water vapour pressure 4 –296.80 67.49
ʻIndividualʼ and ʻday of the yearʼ were included as random factors. d, number of parameters including random factors; AIC, difference between AIC with the
best model.
THE JOURNAL OF EXPERIMENTAL BIOLOGY
Selective brain cooling in Arabian oryx 3923
(Fig.3; Table2). It remains to be seen whether subordinate oryx limit of about 1°C to selective brain cooling in free-living artiodactyls.
have the capacity to further increase the frequency of selective brain Because the hypothalamus is sensitive to changes in temperature of
cooling above 87% or whether they are capable of increasing the a few tenths of a degree (Kuhnen, 1997), such selective brain cooling
magnitude of selective brain cooling as conditions get hotter and would be sufficient to suppress evaporative cooling and therefore
drier seasonally. Other species capable of selective brain cooling reduce water loss. Since selective brain cooling does not disrupt other
increase the magnitude of selective brain cooling during conditions homeostatic systems, it may provide an economical form of autonomic
of water deprivation and heat stress, as shown in both laboratory- thermoregulation. The carotid rete may ultimately provide artiodactyls
housed sheep (Fuller et al., 2007) and Bedouin goats (Jessen et al., with greater acclimatization potential to the hot and dry conditions
1997; Jessen et al., 1998). Compared with euhydration, dehydrated predicted to occur in the future.
goats and sheep increased selective brain cooling with no alteration
in the threshold body temperature at which selective brain cooling ACKNOWLEDGEMENTS
was implemented. When animals were not heat stressed and were We thank the Saudi Wildlife Commission, Riyadh, Saudi Arabia, in particular the
able to lose heat through non-evaporative avenues, two restrained director His Royal Highness Prince Saud Al Faisal, the current secretary-general,
HH Prince Bander Bin Saud, and the secretary-general at the time the study was
camels at rest showed no obvious difference in brain and blood
conducted, Professor A. H. Abuzinada, for supporting the research. From the
temperatures between hydrated and dehydrated states (Schroter et National Wildlife Research Center (NWRC), we are grateful to Dr Saud
al., 1989). Anagariyah for his support in capturing the oryx, and the current director, Ahmad
Al Bouq. In addition, we thank the Mahazat as-Sayd Protected Area rangers for
We conclude that the Arabian oryx uses selective brain cooling
monitoring the animals, and the mammal keepers at NWRC for their help with
to facilitate homeostasis in hot and dry environments. Arid-zone animal handling and assistance during surgery. We thank Dr Jodie Martin and Dr
mammals possessing a carotid rete may employ selective brain Benjamin Rey for assistance with the mixed effects linear models.
cooling to attenuate thermal drive by reducing brain temperature,
which reduces evaporative heat loss and ultimately conserves water FUNDING
by transferring cooling to non-evaporative means (Kuhnen, 1997; This research was funded by the National Research Foundation, South Africa, the
University of the Witwatersrand Medical Faculty Research Endowment Fund
Jessen, 1998; Jessen, 2001; Mitchell et al., 2002). Our oryx, like
(HETE007) and START/PACOM African PhD fellowship awarded to R.S.H.
free-living eland [Tragelaphus oryx(Fuller et al., 1999)], gemsbok
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